Involvement of Fenton chemistry in rice straw degradation by the lignocellulolytic bacterium Pantoea ananatis Sd-1

Abstract

BackgroundLignocellulolytic bacteria have revealed to be a promising source for biofuel production, yet the underlying mechanisms are still worth exploring. Our previous study inferred that the highly efficient lignocellulose degradation by bacterium Pantoea ananatis Sd-1 might involve Fenton chemistry (Fe2+ + H2O2 + H+ → Fe3+ + OH· + H2O), similar to that of white-rot and brown-rot fungi. The aim of this work is to investigate the existence of this Fenton-based oxidation mechanism in the rice straw degradation process of P. ananatis Sd-1.ResultsAfter 3 days incubation of unpretreated rice straw with P. ananatis Sd-1, the percentage in weight reduction of rice straw as well as its cellulose, hemicellulose, and lignin components reached 46.7, 43.1, 42.9, and 37.9 %, respectively. The addition of different hydroxyl radical scavengers resulted in a significant decline (P < 0.001) in rice straw degradation. Pyrolysis gas chromatography–mass spectrometry and Fourier transform infrared spectroscopy analysis revealed the consistency of chemical changes of rice straw components that exists between P. ananatis Sd-1 and Fenton reagent treatment. In addition to the increased total iron ion concentration throughout the rice straw decomposition process, the Fe3+-reducing capacity of P. ananatis Sd-1 was induced by rice straw and predominantly contributed by aromatic compounds metabolites. The transcript levels of the glucose-methanol-choline oxidoreductase gene related to hydrogen peroxide production were significantly up-regulated (at least P < 0.01) in rice straw cultures. Higher activities of GMC oxidoreductase and less hydrogen peroxide concentration in rice straw cultures relative to glucose cultures may be responsible for increasing rice straw degradation, which includes Fenton-like reactions.ConclusionsOur results confirmed the Fenton chemistry-assisted degradation model in P. ananatis Sd-1. We are among the first to show that a Fenton-based oxidation mechanism exists in a bacteria degradation system, which provides a new perspective for how natural plant biomass is decomposed by bacteria. This degradative system may offer an alternative approach to the fungi system for lignocellulosic biofuels production.Electronic supplementary materialThe online version of this article (doi:10.1186/s13068-016-0623-x) contains supplementary material, which is available to authorized users.

Oxidoreductases and Reactive Oxygen Species in Conversion of Lignocellulosic Biomass

“…Similarly, Fentontype reactions were shown to occur in the midgut of a leaf-feeding caterpillar (254). It is also worth noting that the use of a Fenton-like system during biomass decomposition has recently been described for a bacterium (255).…”

Multiplicity of enzymatic functions in the CAZy AA3 family

“…The majority of these putative bacterial POx sequences occurred in the phylum of Actinobacteria . POx from Arthrobacter siccitolerans is the only characterized bacterial POx so far (Mendes et al 2016 ), but POx activity was also proven in medium of the endophytic bacterium Pantoea ananatis when cultivated on rice straw (Ma et al 2016a ) suggesting that POx might be further spread throughout the bacterial domain.…”

“…These are typically found in the genomes of brown-rot organisms, in contrast to the other oxidases implicated in peroxide formation in wood-degrading fungi, AAO and POx (Lundell et al 2014 ). Recently, Fenton chemistry was also suggested to play a role in the degradation of rice straw by the endophytic bacterium Pantoea ananatis (Ma et al 2016a ). Strain P. ananatis Sd-1 was found to contain nine genes for AA enzymes, significantly more than the genomes of other P. ananatis isolates (Ma et al 2016b ).…”

Lignin induced iron reduction by novel sp., Tolumonas lignolytic BRL6-1

“…We investigated to see if BRL6-1 secreted lignolytic enzymes or iron reducing proteins in the presence of lignin as seen for aerobic fungi and bacteria [12,13,15]. Samples from late stationary phase were run on an SDS-PAGE and silver stained to detect differential banding between the two growth conditions.…”

“…Under oxic conditions, enzymes such as laccases and peroxidases produce oxidants that diffuse into and reduce the lignin complex [9,11], causing bond scission reactions between lignin subunits. For microorganisms that lack lignolytic enzymes such as brown-rot fungi as well as aerobic bacteria like Pantoea ananatis Sd-1 and Cupriavidus basilensis B-8, chelator-mediated Fenton chemistry (CMF) is used to depolymerize lignin [12][13][14][15]. In this mechanism, the microorganism produces an iron reducing molecule, a chelator molecule, and H 2 O 2 .…”